Hybrid allele‑specific ChIP‑seq analysis identifies variation in brassinosteroid‑responsive transcription factor binding linked to traits in maize

Authors

Thomas Hartwig, Carnegie Institution for Science, Heinrich-Heine University, Max Planck Institute for Plant Breeding Research
Michael Banf, Carnegie Institution for Science
Gisele Passaia Prietsch, Carnegie Institution for Science
Jia‑Ying Zhu, Leibniz-Institute of Plant Genetics and Crop Plant Research
Isabel Mora‑Ramírez, Leibniz-Institute of Plant Genetics and Crop Plant Research
Jos H. M. Schippers, Leibniz-Institute of Plant Genetics and Crop Plant Research
Samantha J. Snodgrass, Iowa State University
Arun S. Seetharam, Iowa State University
Bruno Huettel, Max Planck Institute for Plant Breeding Research
Judith M. Kolkman, Cornell University
Jiashi Yang, University of Nebraska-LincolnFollow
Julia Engelhorn, Heinrich-Heine University, Max Planck Institute for Plant Breeding Research
Zhi‑Yong Wang, Carnegie Institution for Science

Document Type

Article

Date of this Version

5-8-2023

Citation

Hartwig et al. Genome Biology (2023) 24:108 https://doi.org/10.1186/s13059-023-02909-w

Comments

Open access.

Abstract

Background: Genetic variation in regulatory sequences that alter transcription factor (TF) binding is a major cause of phenotypic diversity. Brassinosteroid is a growth hormone that has major effects on plant phenotypes. Genetic variation in brassinosteroidresponsive cis-elements likely contributes to trait variation. Pinpointing such regulatory variations and quantitative genomic analysis of the variation in TF-target binding, however, remains challenging. How variation in transcriptional targets of signaling pathways such as the brassinosteroid pathway contributes to phenotypic variation is an important question to be investigated with innovative approaches.

Results: Here, we use a hybrid allele-specific chromatin binding sequencing (HASChseq) approach and identify variations in target binding of the brassinosteroid-responsive TF ZmBZR1 in maize. HASCh-seq in the B73xMo17 F1s identifies thousands of target genes of ZmBZR1. Allele-specific ZmBZR1 binding (ASB) has been observed for 18.3% of target genes and is enriched in promoter and enhancer regions. About a quarter of the ASB sites correlate with sequence variation in BZR1-binding motifs and another quarter correlate with haplotype-specific DNA methylation, suggesting that both genetic and epigenetic variations contribute to the high level of variation in ZmBZR1 occupancy. Comparison with GWAS data shows linkage of hundreds of ASB loci to important yield and disease-related traits.

Conclusion: Our study provides a robust method for analyzing genome-wide variations of TF occupancy and identifies genetic and epigenetic variations of the brassinosteroid response transcription network in maize.